Remodeling T cell compartments during anti-CD3 immunotherapy of type 1 diabetes

Cellular Immunology

Volumn 319, Issue , 2017, Pages 3-9

  Long, S Alice ^a   Thorpe, Jerill ^a   Herold, Kevan C ^b   Ehlers, Mario ^c   Sanda, Srinath ^c   Lim, Noha ^d   Linsley, Peter S ^a   Nepom, Gerald T ^a,d   Harris, Kristina M ^d  

^a BENAROYA RESEARCH INSTITUTE   (United States)

^b YALE UNIVERSITY   (United States)

^c Immune Tolerance Network   (United States)

^d Immune Tolerance Network   (United States)

Author keywords

Anti CD3 monoclonal antibody; Immune tolerance; Immunotherapy; T cell inactivation; T lymphocyte; Type 1 diabetes

Indexed keywords

CD4 ANTIGEN; CD57 ANTIGEN; INTERLEUKIN 7 RECEPTOR; PROGRAMMED DEATH 1 LIGAND 1; TEPLIZUMAB; TRANSCRIPTION FACTOR FOXP3; ANTIDIABETIC AGENT; C PEPTIDE; CD3 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; IMMUNOGLOBULIN RECEPTOR; INTERLEUKIN 7 RECEPTOR ALPHA; KLRG1 PROTEIN, HUMAN; LECTIN; MONOCLONAL ANTIBODY; PDCD1 PROTEIN, HUMAN; PROGRAMMED DEATH 1 RECEPTOR; TIGIT PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN;

ADOLESCENT; ADULT; ARTICLE; BLOOD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLS BY BODY ANATOMY; CHILD; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOTHERAPY; INSULIN DEPENDENT DIABETES MELLITUS; MODULATION; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; AGONISTS; DIABETES MELLITUS, TYPE 1; DRUG EFFECTS; FEMALE; GENE EXPRESSION; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; IMMUNOMODULATION; MALE; PATHOLOGY; PROCEDURES; RANDOMIZED CONTROLLED TRIAL;

ADOLESCENT; ADULT; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD3; ANTIGENS, CD57; C-PEPTIDE; CD8-POSITIVE T-LYMPHOCYTES; CHILD; DIABETES MELLITUS, TYPE 1; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; HUMANS; HYPOGLYCEMIC AGENTS; IMMUNE TOLERANCE; IMMUNOMODULATION; IMMUNOTHERAPY; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; LECTINS, C-TYPE; MALE; PROGRAMMED CELL DEATH 1 RECEPTOR; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTES, REGULATORY; TRANS-ACTIVATORS;

EID: 85028331021     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2017.07.007     Document Type: Article

References (35)

1. Herold, K.C., Hagopian, W., Auger, J.A., Poumian-Ruiz, E., Taylor, L., Donaldson, D., Gitelman, S.E., Harlan, D.M., Xu, D., Zivin, R.A., Bluestone, J.A., Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. N. Engl. J. Med. 346 (2002), 1692–1698.
2. Herold, K.C., Gitelman, S.E., Ehlers, M.R., Gottlieb, P.A., Greenbaum, C.J., Hagopian, W., Boyle, K.D., Keyes-Elstein, L., Aggarwal, S., Phippard, D., Sayre, P.H., McNamara, J., Bluestone, J.A., Teplizumab (anti-CD3 mAb) treatment preserves C-peptide responses in patients with new-onset type 1 diabetes in a randomized controlled trial: metabolic and immunologic features at baseline identify a subgroup of responders. Diabetes 62 (2013), 3766–3774.
3. Herold, K.C., Gitelman, S.E., Masharani, U., Hagopian, W., Bisikirska, B., Donaldson, D., Rother, K., Diamond, B., Harlan, D.M., Bluestone, J.A., A single course of anti-CD3 monoclonal antibody hOKT3gamma1(Ala-Ala) results in improvement in C-peptide responses and clinical parameters for at least 2 years after onset of type 1 diabetes. Diabetes 54 (2005), 1763–1769.
4. Masharani, U.B., Becker, J., Teplizumab therapy for type 1 diabetes. Expert Opin. Biol. Ther. 10 (2010), 459–465.
5. Sherry, N., Hagopian, W., Ludvigsson, J., Jain, S.M., Wahlen, J., Ferry, R.J. Jr., Bode, B., Aronoff, S., Holland, C., Carlin, D., King, K.L., Wilder, R.L., Pillemer, S., Bonvini, E., Johnson, S., Stein, K.E., Koenig, S., Herold, K.C., Daifotis, A.G., Teplizumab for treatment of type 1 diabetes (Protege study): 1-year results from a randomised, placebo-controlled trial. Lancet 378 (2011), 487–497.
6. Glandt, M., Herold, K.C., Treatment of type 1 diabetes with anti-T-cell agents: from T-cell depletion to T-cell regulation. Curr. Diabetes Rep. 4 (2004), 291–297.
7. Tooley, J.E., Vudattu, N., Choi, J., Cotsapas, C., Devine, L., Raddassi, K., Ehlers, M.R., McNamara, J.G., Harris, K.M., Kanaparthi, S., Phippard, D., Herold, K.C., Changes in T-cell subsets identify responders to FcR-nonbinding anti-CD3 mAb (teplizumab) in patients with type 1 diabetes. Eur. J. Immunol. 46 (2016), 230–241.
8. Long, S.A., Thorpe, J., DeBerg, H.A., Gersuk, V., Eddy, J.A., Harris, K.M., Ehlers, M., Herold, K.C., Nepom, G.T., Linsley, P.S., Partial exhaustion of CD8 T cells and clinical response to teplizumab in new-onset type 1 diabetes. Sci. Immunol., 1, 2016, eaai7793.
9. Wallberg, M., Recino, A., Phillips, J., Howie, D., Vienne, M., Paluch, C., Azuma, M., Wong, F.S., Waldmann, H., Cooke, A., Anti-CD3 treatment up-regulates programmed cell death protein-1 expression on activated effector T cells and severely impairs their inflammatory capacity. Immunology, 2017.
10. Penaranda, C., Tang, Q., Bluestone, J.A., Anti-CD3 therapy promotes tolerance by selectively depleting pathogenic cells while preserving regulatory T cells. J. Immunol. 187 (2011), 2015–2022.
11. Ablamunits, V., Bisikirska, B., Herold, K.C., Acquisition of regulatory function by human CD8(+) T cells treated with anti-CD3 antibody requires TNF. Eur. J. Immunol. 40 (2010), 2891–2901.
12. Waldron-Lynch, F., Henegariu, O., Deng, S., Preston-Hurlburt, P., Tooley, J., Flavell, R., Herold, K.C., Teplizumab induces human gut-tropic regulatory cells in humanized mice and patients. Sci. Transl. Med., 4, 2012, 118ra112.
13. Valle, A., Barbagiovanni, G., Jofra, T., Stabilini, A., Perol, L., Baeyens, A., Anand, S., Cagnard, N., Gagliani, N., Piaggio, E., Battaglia, M., Heterogeneous CD3 expression levels in differing T cell subsets correlate with the in vivo anti-CD3-mediated T cell modulation. J. Immunol. 194 (2015), 2117–2127.
14. Wherry, E.J., Kurachi, M., Molecular and cellular insights into T cell exhaustion. Nat. Rev. Immunol. 15 (2015), 486–499.
15. Crespo, J., Sun, H., Welling, T.H., Tian, Z., Zou, W., T cell anergy, exhaustion, senescence, and stemness in the tumor microenvironment. Curr. Opin. Immunol. 25 (2013), 214–221.
16. Schietinger, A., Greenberg, P.D., Tolerance and exhaustion: defining mechanisms of T cell dysfunction. Trends Immunol. 35 (2014), 51–60.
17. Zehn, D., Wherry, E.J., Immune memory and exhaustion: clinically relevant lessons from the LCMV model. Adv. Exp. Med. Biol. 850 (2015), 137–152.
18. McKinney, E.F., Lee, J.C., Jayne, D.R., Lyons, P.A., Smith, K.G., T-cell exhaustion, co-stimulation and clinical outcome in autoimmunity and infection. Nature 523 (2015), 612–616.
19. Lang, K.S., Recher, M., Navarini, A.A., Harris, N.L., Lohning, M., Junt, T., Probst, H.C., Hengartner, H., Zinkernagel, R.M., Inverse correlation between IL-7 receptor expression and CD8 T cell exhaustion during persistent antigen stimulation. Eur. J. Immunol. 35 (2005), 738–745.
20. Hagopian, W., Ferry, R.J. Jr., Sherry, N., Carlin, D., Bonvini, E., Johnson, S., Stein, K.E., Koenig, S., Daifotis, A.G., Herold, K.C., Ludvigsson, J., Protege, I., Trial, Teplizumab preserves C-peptide in recent-onset type 1 diabetes: two-year results from the randomized, placebo-controlled Protege trial. Diabetes 62 (2013), 3901–3908.
21. Vudattu, N.K., Herold, K.C., Treatment of new onset type 1 diabetes with teplizumab: successes and pitfalls in development. Expert Opin. Biol. Ther. 14 (2014), 377–385.
22. Besancon, A., Baas, M., Goncalves, T., Valette, F., Waldmann, H., Chatenoud, L., You, S., The induction and maintenance of transplant tolerance engages both regulatory and anergic CD4+ T cells. Front. Immunol., 8, 2017, 218.
23. Burton, B.R., Britton, G.J., Fang, H., Verhagen, J., Smithers, B., Sabatos-Peyton, C.A., Carney, L.J., Gough, J., Strobel, S., Wraith, D.C., Sequential transcriptional changes dictate safe and effective antigen-specific immunotherapy. Nat. Commun., 5, 2014, 4741.
24. McPherson, R.C., Konkel, J.E., Prendergast, C.T., Thomson, J.P., Ottaviano, R., Leech, M.D., Kay, O., Zandee, S.E., Sweenie, C.H., Wraith, D.C., Meehan, R.R., Drake, A.J., Anderton, S.M., Epigenetic modification of the PD-1 (Pdcd1) promoter in effector CD4(+) T cells tolerized by peptide immunotherapy. Elife, 3, 2014.
25. Keir, M.E., Francisco, L.M., Sharpe, A.H., PD-1 and its ligands in T-cell immunity. Curr. Opin. Immunol. 19 (2007), 309–314.
26. Freeman, G.J., Long, A.J., Iwai, Y., Bourque, K., Chernova, T., Nishimura, H., Fitz, L.J., Malenkovich, N., Okazaki, T., Byrne, M.C., Horton, H.F., Fouser, L., Carter, L., Ling, V., Bowman, M.R., Carreno, B.M., Collins, M., Wood, C.R., Honjo, T., Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192 (2000), 1027–1034.
27. Boussiotis, V.A., Chatterjee, P., Li, L., Biochemical signaling of PD-1 on T cells and its functional implications. Cancer J. 20 (2014), 265–271.
28. Barber, D.L., Wherry, E.J., Masopust, D., Zhu, B., Allison, J.P., Sharpe, A.H., Freeman, G.J., Ahmed, R., Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439 (2006), 682–687.
29. Asano, T., Meguri, Y., Yoshioka, T., Kishi, Y., Iwamoto, M., Nakamura, M., Sando, Y., Yagita, H., Koreth, J., Kim, H.T., Alyea, E.P., Armand, P., Cutler, C.S., Ho, V.T., Antin, J.H., Soiffer, R.J., Maeda, Y., Tanimoto, M., Ritz, J., Matsuoka, K.I., PD-1 modulates regulatory T-cell homeostasis during low-dose interleukin-2 therapy. Blood 129 (2017), 2186–2197.
30. Lee, L.F., Logronio, K., Tu, G.H., Zhai, W., Ni, I., Mei, L., Dilley, J., Yu, J., Rajpal, A., Brown, C., Appah, C., Chin, S.M., Han, B., Affolter, T., Lin, J.C., Anti-IL-7 receptor-alpha reverses established type 1 diabetes in nonobese diabetic mice by modulating effector T-cell function. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), 12674–12679.
31. Penaranda, C., Kuswanto, W., Hofmann, J., Kenefeck, R., Narendran, P., Walker, L.S., Bluestone, J.A., Abbas, A.K., Dooms, H., IL-7 receptor blockade reverses autoimmune diabetes by promoting inhibition of effector/memory T cells. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), 12668–12673.
32. Cernea, S., Herold, K.C., Monitoring of antigen-specific CD8 T cells in patients with type 1 diabetes treated with antiCD3 monoclonal antibodies. Clin. Immunol. 134 (2010), 121–129.
33. Herold, K.C., Gitelman, S., Greenbaum, C., Puck, J., Hagopian, W., Gottlieb, P., Sayre, P., Bianchine, P., Wong, E., Seyfert-Margolis, V., Bourcier, K., Bluestone, J.A., I.T.N.A.I.S.G. Immune Tolerance Network, Treatment of patients with new onset Type 1 diabetes with a single course of anti-CD3 mAb Teplizumab preserves insulin production for up to 5 years. Clin. Immunol. 132 (2009), 166–173.
34. Huang, A.C., Postow, M.A., Orlowski, R.J., Mick, R., Bengsch, B., Manne, S., Xu, W., Harmon, S., Giles, J.R., Wenz, B., Adamow, M., Kuk, D., Panageas, K.S., Carrera, C., Wong, P., Quagliarello, F., Wubbenhorst, B., D'Andrea, K., Pauken, K.E., Herati, R.S., Staupe, R.P., Schenkel, J.M., McGettigan, S., Kothari, S., George, S.M., Vonderheide, R.H., Amaravadi, R.K., Karakousis, G.C., Schuchter, L.M., Xu, X., Nathanson, K.L., Wolchok, J.D., Gangadhar, T.C., Wherry, E.J., T-cell invigoration to tumour burden ratio associated with anti-PD-1 response. Nature, 2017.
35. Manieri, N.A., Chiang, E.Y., Grogan, J.L., TIGIT: a key inhibitor of the cancer immunity cycle. Trends Immunol. 38 (2017), 20–28.